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Reconstruction of the ancestral marsupial karyotype from comparative gene maps.

Deakin JE, Delbridge ML, Koina E, Harley N, Alsop AE, Wang C, Patel VS, Graves JA - BMC Evol. Biol. (2013)

Bottom Line: Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.Our physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor.Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

View Article: PubMed Central - HTML - PubMed

Affiliation: ARC Centre of Excellence for Kangaroo Genomics, Canberra, Australia. janine.deakin@canberra.edu.au.

ABSTRACT

Background: The increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian (marsupial and eutherian) mammals. However, the reconstruction of ancestral genomes requires genome assemblies to be anchored to chromosomes. The recently sequenced tammar wallaby (Macropus eugenii) genome was assembled into over 300,000 contigs. We previously devised an efficient strategy for mapping large evolutionarily conserved blocks in non-model mammals, and applied this to determine the arrangement of conserved blocks on all wallaby chromosomes, thereby permitting comparative maps to be constructed and resolve the long debated issue between a 2n = 14 and 2n = 22 ancestral marsupial karyotype.

Results: We identified large blocks of genes conserved between human and opossum, and mapped genes corresponding to the ends of these blocks by fluorescence in situ hybridization (FISH). A total of 242 genes was assigned to wallaby chromosomes in the present study, bringing the total number of genes mapped to 554 and making it the most densely cytogenetically mapped marsupial genome. We used these gene assignments to construct comparative maps between wallaby and opossum, which uncovered many intrachromosomal rearrangements, particularly for genes found on wallaby chromosomes X and 3. Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.

Conclusions: Our physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor. Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

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The predicted ancestral therian chromosome containing segments C10, C11 and C12 and the derivation of opossum and wallaby chromosomes. (A) The predicted therian ancestral chromosome aligned against chicken chromosomes containing C10, C11 and C12 genes. An inversion and the addition of genes corresponding to part of human chromosomes 1 and 19 to the distal end of this chromosome and two more inversion events result in a putative marsupial ancestral chromosome consisting of all three segments in the order of C10, C12 and C11. Opossum (MDO) chromosomes 4 and 7 are derived from a fission event taking place in segment C12. (B) Wallaby (MEU) chromosomes 5 and 6 are derived from the predicted marsupial ancestor via inversions, a fission between C10 and C12 and a further inversion within C11.
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Figure 7: The predicted ancestral therian chromosome containing segments C10, C11 and C12 and the derivation of opossum and wallaby chromosomes. (A) The predicted therian ancestral chromosome aligned against chicken chromosomes containing C10, C11 and C12 genes. An inversion and the addition of genes corresponding to part of human chromosomes 1 and 19 to the distal end of this chromosome and two more inversion events result in a putative marsupial ancestral chromosome consisting of all three segments in the order of C10, C12 and C11. Opossum (MDO) chromosomes 4 and 7 are derived from a fission event taking place in segment C12. (B) Wallaby (MEU) chromosomes 5 and 6 are derived from the predicted marsupial ancestor via inversions, a fission between C10 and C12 and a further inversion within C11.

Mentions: The ancestral arrangement of these three conserved segments is easily reconstructed by comparing the chicken gene arrangement with that in the two marsupials (Figure 7). The ancestral therian chromosome, consisting of segments C10, C12, C11, can be easily derived by adding genes from chicken chromosomes 7 (HSA2 and 3 genes), 9 (HSA2 and 3) and 24 (HSA11) to the distal end of chicken chromosome 1. By using the chicken gene order as a guide, the marsupial ancestral chromosome could have been formed by two large and two smaller inversions, resulting in the ancestral arrangement C10-C12-C11. Opossum chromosomes 4 and 7 would be the result of a fission event between HSA3 and 21 genes (Figure 7A). Wallaby chromosomes 5 and 6 are also easily derived from our predicted ancestral chromosome, with two inversions rearranging genes in C12 and fission separating C10 from C12 (Figure 7B). Subsequent intrachromosomal rearrangements, occurring after wallaby/opossum divergence, account for the current arrangement of C11 genes in these two species.


Reconstruction of the ancestral marsupial karyotype from comparative gene maps.

Deakin JE, Delbridge ML, Koina E, Harley N, Alsop AE, Wang C, Patel VS, Graves JA - BMC Evol. Biol. (2013)

The predicted ancestral therian chromosome containing segments C10, C11 and C12 and the derivation of opossum and wallaby chromosomes. (A) The predicted therian ancestral chromosome aligned against chicken chromosomes containing C10, C11 and C12 genes. An inversion and the addition of genes corresponding to part of human chromosomes 1 and 19 to the distal end of this chromosome and two more inversion events result in a putative marsupial ancestral chromosome consisting of all three segments in the order of C10, C12 and C11. Opossum (MDO) chromosomes 4 and 7 are derived from a fission event taking place in segment C12. (B) Wallaby (MEU) chromosomes 5 and 6 are derived from the predicted marsupial ancestor via inversions, a fission between C10 and C12 and a further inversion within C11.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4222502&req=5

Figure 7: The predicted ancestral therian chromosome containing segments C10, C11 and C12 and the derivation of opossum and wallaby chromosomes. (A) The predicted therian ancestral chromosome aligned against chicken chromosomes containing C10, C11 and C12 genes. An inversion and the addition of genes corresponding to part of human chromosomes 1 and 19 to the distal end of this chromosome and two more inversion events result in a putative marsupial ancestral chromosome consisting of all three segments in the order of C10, C12 and C11. Opossum (MDO) chromosomes 4 and 7 are derived from a fission event taking place in segment C12. (B) Wallaby (MEU) chromosomes 5 and 6 are derived from the predicted marsupial ancestor via inversions, a fission between C10 and C12 and a further inversion within C11.
Mentions: The ancestral arrangement of these three conserved segments is easily reconstructed by comparing the chicken gene arrangement with that in the two marsupials (Figure 7). The ancestral therian chromosome, consisting of segments C10, C12, C11, can be easily derived by adding genes from chicken chromosomes 7 (HSA2 and 3 genes), 9 (HSA2 and 3) and 24 (HSA11) to the distal end of chicken chromosome 1. By using the chicken gene order as a guide, the marsupial ancestral chromosome could have been formed by two large and two smaller inversions, resulting in the ancestral arrangement C10-C12-C11. Opossum chromosomes 4 and 7 would be the result of a fission event between HSA3 and 21 genes (Figure 7A). Wallaby chromosomes 5 and 6 are also easily derived from our predicted ancestral chromosome, with two inversions rearranging genes in C12 and fission separating C10 from C12 (Figure 7B). Subsequent intrachromosomal rearrangements, occurring after wallaby/opossum divergence, account for the current arrangement of C11 genes in these two species.

Bottom Line: Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.Our physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor.Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

View Article: PubMed Central - HTML - PubMed

Affiliation: ARC Centre of Excellence for Kangaroo Genomics, Canberra, Australia. janine.deakin@canberra.edu.au.

ABSTRACT

Background: The increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian (marsupial and eutherian) mammals. However, the reconstruction of ancestral genomes requires genome assemblies to be anchored to chromosomes. The recently sequenced tammar wallaby (Macropus eugenii) genome was assembled into over 300,000 contigs. We previously devised an efficient strategy for mapping large evolutionarily conserved blocks in non-model mammals, and applied this to determine the arrangement of conserved blocks on all wallaby chromosomes, thereby permitting comparative maps to be constructed and resolve the long debated issue between a 2n = 14 and 2n = 22 ancestral marsupial karyotype.

Results: We identified large blocks of genes conserved between human and opossum, and mapped genes corresponding to the ends of these blocks by fluorescence in situ hybridization (FISH). A total of 242 genes was assigned to wallaby chromosomes in the present study, bringing the total number of genes mapped to 554 and making it the most densely cytogenetically mapped marsupial genome. We used these gene assignments to construct comparative maps between wallaby and opossum, which uncovered many intrachromosomal rearrangements, particularly for genes found on wallaby chromosomes X and 3. Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.

Conclusions: Our physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor. Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

Show MeSH
Related in: MedlinePlus